The Church is steeped in history! The Nave was built in the early 12th century which is shown in the sloping inner walls which are made of rubble masonry (inner and outer stone filled with rubble) and the walls have remained for almost 900 years. The Chancel was built in the 13th century and the style of the lancet window is typical of the era.

The Tower was built in the 14th century; the single bell in the Tower is dated 1795. The Church was refurbished in the 14th century by Gilbert de Ayton – though no-one knows why.

In the 15th century, the Nave walls were raised and buttresses added and the present square-headed windows are probably from the same time period. The Porch was added in the 17th century with a date stone showing 1634. Major repairs were carried out in the 18th century (1721) under Archdeacon Henage Dering, which included raising the North Wall.

The 19th century saw another major inside repair with 10 seats being provided and the Gallery taken down. In 1901, the Vestry was built being paid for by Rev J C Simpson of Ayton Lodge (a retired clergyman and one of a series of families who lived at the Lodge). This 1901 Vestry, was demolished in 2006 and replaced by the new Church room. The Priests’ Door is in the south wall of the Chancel, but it is blocked off on the inside and there is evidence of a similar-sized door on the North wall of the Nave.

In the midst of the 19th century, cement rendering was added but removed in the 20th century, though some small patches of rendering remain – the removal of most of the rendering has resulted in erosion of some of the rather soft stone since and is causing great concern for those responsible maintenance of the building.

For up to 650 years, the Church stood in a field with residents of the East and West Ayton being buried in Seamer or Hutton Buscel graveyards. The graveyard at St John’s was walled in 1887 and consecrated by the Archbishop of York in 1888. The first person to be buried in the grounds of the Church was Elizabeth Buckle who passed away in October 1887. The Rev Simpson was also buried in the graveyard in 1903, and his wife who passed away in 1919 is also buried in the grounds of the Church.

The main door to the Church has a “beakhead” arch showing nine raven heads, each rumoured to be different from the others; there are also fine, symbolic markings.

The Font, which is early Norman has been in use for over 800 years and has been dated at around 1130. The shallow design is typical of the time and is made from one single stone block; round the top of the Font it is evident that two pieces of stone have been broken off. One of the hollows reveals a piece of iron from when Holy Water used to be kept in the Font covered with a locked lid; the lid was wrenched off by objectors which left the iron piece behind.

Just inside the main door of the Church is a hole; this hole was used to house a balk of wood in times of danger when Villagers sought sanctuary within the Church. A second (smaller) hole can be found slightly west of the door which is thought to have housed a repository for the chrismatory (a vessel holding the Holy oil) or the hole could have held a statue support.

Most of the furniture (pulpit, lectern, etc) was bought by monies given or raised by several families who lived in Ayton Lodge whilst other items (choir stalls and altar rails) are memorials from earlier in the 20th century.  The stained glass window, another memorial, is a good example of the 20th century. There is a pronounced “bulge” on the inside (only) it is a mystery as to what lies under the “bulge”; it is located over the top of the blocked up North door.

East Ayton became a separate Parish in it’s own right in 1982, but is within the joint Benefice of Seamer and East Ayton.